Abstract
Geosmithia species (Hypocreales, Ascomycota) are associates of bark beetles and other arthropods. One species, Geosmithia morbida, is a virulent tree pathogen of Juglans nigra. To date, 10 Geosmithia spp. from conifer-infesting, and at least 23 species from hardwood associated bark beetles have been reported from Europe. The aim of this study was to survey Geosmithia spp. associated with 18 bark and ambrosia beetle species in hardwood ecosystems in Poland. In addition, we evaluated the pathogenicity of the six Geosmithia species by inoculating Acer, Fagus, Quercus, Tilia and Ulmus seedlings. Our surveys yielded a total of 1060 isolates from 2915 beetles and 1887 galleries. We identified isolates using morphology and ITS, β-tubulin and TEF1-α sequences. Altogether we identified 11 species including nine previously known and two new species described here as Geosmithia fagi sp. nov. and G. pazoutovae sp. nov. In addition, a sister species G. longistipitata sp. nov., associated with Picea trees, is described here. Bark beetles from hardwoods, with exeption of Dryocoetes alni, D. villosus, Scolytus ratzeburgi and ambrosia beetles, appear to be regular vectors of Geosmithia spp. Like in other parts of the world, most Geosmithia taxa exhibited a distinct level of vector/host specificity. None of Geosmithia isolates induced any disease symptoms under the conditions of our experiment. This study highlights the need for more intensive surveys across additional areas of Central and Northern Europe, insect vectors and host tree species in order to elucidate the Geosmithia species diversity in this region.
Similar content being viewed by others
References
Crous P, Luangsa-Ard J, Wingfield M, Carnegie A, Hernández-Restrepo M, Lombard L, Roux J, Barreto R, Baseia I, Cano-Lira J (2018) Fungal Planet description sheets. Persoonia Molecular Phylogeny and Evolution of Fungi: 785–867 41:238
Dori-Bachash M, Avrahami-Moyal L, Protasov A, Mendel Z, Freeman S (2015) The occurrence and pathogenicity of Geosmithia spp. and common blue-stain fungi associated with pine bark beetles in planted forests in Israel. Eur J Plant Pathol 143:627–639
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes—application to the identification of mycorrhiza and rusts. Mol Ecol 2:113–118
Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. App Environ Microb 61:1323–1330
Huang Y-T, Kolařík M, Kasson MT, Hulcr J (2017) Two new Geosmithia species in G. pallida species complex from bark beetles in eastern USA. Mycologia 109:790–803
Huang Y-T, Skelton J, Johnson AJ, Kolařík M, Hulcr J (2019) Geosmithia species in southeastern USA and their affinity to beetle vectors and tree hosts. Fungal Ecol 39:168–183
Jankowiak R, Bilański P (2018) Geosmithia species associated with fir-infesting beetles in Poland. Acta Mycol 53(2):1115. https://doi.org/10.5586/am.1115
Jankowiak R, Kolařík M (2010) Fungi associated with the fir bark beetle Cryphalus piceae in Poland. Forest Pathol 40:133–144
Jankowiak R, Rossa R (2008) Associations between Pityogenes bidentatus and fungi in young managed Scots pine stands in Poland. Forest Pathol 38:169–177
Jankowiak R, Kolaŕík M, Bilański P (2014) Association of Geosmithia fungi (Ascomycota: Hypocreales) with pine- and spruce-infesting bark beetles in Poland. Fungal Ecol 11:71–79
Jankowiak R, Strzałka B, Bilański P, Kacprzyk M, Lukášová K, Linnakoski R, Matwiejczuk S, Misztela M, Rossa R (2017) Diversity of Ophiostomatales species associated with conifer-infesting beetles in the Western Carpathians. Eur J Forest Res 136:939–956
Jankowiak R, Strzałka B, Bilański P, Kacprzyk M, Wieczorek P, Linnakoski R (2019) Ophiostomatoid fungi associated with hardwood-infesting bark and ambrosia beetles in Poland: taxonomic diversity and vector specificity. Fungal Ecol 39:152–167
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Kirisits T (2004) Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. In: Lieutier F, Day KR, Battisti A (eds) Bark and wood boring insects in living trees in Europe, a synthesis. Kluwer, Dordrecht, pp 185–223
Kirschner R (2001) Diversity of filamentous fungi in bark beetle galleries in central Europe. In: Misra JK, Horn BW (eds) Trichomycetes and Other Fungal Groups. Trichomycetes and Other Fungal Groups. Robert W. Lichtwardt Commemoration Volume, Robert W, pp 175–196
Kolařík M, Jankowiak R (2013) Vector affinity and diversity of Geosmithia fungi living on subcortical insects inhabiting Pinaceae species in Central and Northeastern Europe. Microb Ecol 66:682–700
Kolařík M, Kirkendall LR (2010) Evidence for a new lineage of primary ambrosia fungi in Geosmithia Pitt (Ascomycota: Hypocreales). Fungal Biol 114:676–689
Kolařik M, Kubátová A, Hulcr J, Pažoutová S (2008) Geosmithia fungi are highly diverse and consistent bark beetle associates: evidence from their community structure in temperate Europe. Microb Ecol 55:65–80
Kolařík M, Kubátová A, Pazoutova S, Šrutka P (2004) Morphological and molecular characterisation of Geosmithia putterillii, G. pallida comb. nov. and G. flava sp. nov., associated with subcorticolous insects. Mycol Res 108:1053–1069
Kolařík M, Kubátová A, Cepicka I, Pazoutova S, Šrutka P (2005) A complex of three new white-spored, sympatric, and host range limited Geosmithia species. Mycol Res 109:1323–1336
Kolařík M, Kostovčík M, Pazoutova S (2007) Host range and diversity of the genus Geosmithia (Ascomycota: Hypocreales) living in association with bark beetles in the Mediterranean area. Mycol Res 111:1298–1310
Kolařík M, Freeland E, Utley C, Tisserat N (2011) Geosmithia morbida sp. nov., a new phytopathogenic species living in symbiosis with the walnut twig beetle (Pityophthorus juglandis) on Juglans in USA. Mycologia 103:325–332
Kolařík M, Hulcr J, Kirkendall LR (2015) New species of Geosmithia and Graphium associated with ambrosia beetles in Costa Rica. Czech Mycol 67:29–35
Kolařík M, Hulcr J, Tisserat N, De Beer W, Kostovčík M, Kolaříková Z, Seybold SJ, Rizzo D (2017) Geosmithia associated with bark beetles and woodborers in the western USA: taxonomic diversity and vector specificity. Mycologia 109:185–199
Kornerup A, Wanscher JH (1978) Methuen Handbook of Colour, 3rd edn. Eyre Methuen, London
Krokene P, Solheim H (1998) Assessing the virulence of four bark beetle associated blue-stain fungi using Norway spruce seedlings. Plant Pathol 47:537–540
Kubátová A, Kolařík M, Prášil K, Novotný D (2004) Bark beetles and their galleries: well-known niche for little known fungi, case of Geosmithia. Czech Mycol 55:1–18
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Lamarche J, Potvin A, Pelletier G, Stewart D, Feau N, Alayon DI, Dale AL, Coelho A, Uzunović A, Bilodeau GJ (2015) Molecular detection of 10 of the most unwanted alien forest pathogens in Canada using real-time PCR. PLoS ONE 10(8):e0134265
Linnakoski R, De Beer ZW, Niemelä P, Wingfield MJ (2012) Associations of conifer-infesting bark beetles and fungi in Fennoscandia. Insects 3:200–227
Lynch SC, Wang DH, Mayorquin JS, Rugman-Jones P, Stouthamer R, Eskalen A (2014) First report of Geosmithia pallida causing foamy bark canker, a new disease on coast live oak (Quercus agrifolia) in association with Pseudopityophthorus pubipennis in California. Plant Dis 98:1276–1277
Machingambi NM, Roux J, Dreyer LL, Roets F (2014) Bark beetles (Curculionidae: Scolytinae), their phoretic mites (Acari) and associated Geosmithia species (Ascomycota: Hypocreales) from Virgilia trees in South Africa. Fungal Biol 118:472–483
McPherson BA, Erbilgin N, Bonello P, Wood DL (2013) Fungal species assemblages associated with Phytophthora ramorum infected coast live oaks following bark and ambrosia beetle colonization in northern California. For Ecol Manag 291:30–42
Montecchio L, Fanchin G, Simonato M, Faccoli M (2014) First record of thousand cankers disease fungal pathogen Geosmithia morbida and walnut twig beetle Pityophthorus juglandis on Juglans regia in Europe. Plant Dis 98:1445
Nunberg M (1981) Klucze do rozpoznawania owadow Polski [Keys for the identification of Polish Insects]. Część XIX. Chrząszcze-Coleoptera, Korniki—Scolytidae, Wyrynniki—Platypodidae. Zeszyt 99–100, PWN, Warszawa- Wrocław
O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Biol Evol 7:103–116
Pepori AL, Kolařík M, Bettini PP, Vettraino AM, Santini A (2015) Morphological and molecular characterisation of Geosmithia species on European elms. Fungal Biol 119:1063–1074
Pitt JI (1979) Geosmithia gen. nov. for Penicillium lavendulum and related species. Can J Bot 57:2021–2030
Pitt JI, Hocking AD (2009) The ecology of fungal food spoilage. In: Fungi and food spoilage, vol 519. Springer, New York
Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: Evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Seybold SJ, Haugen D, O’Brien J, Graves AD (2013) Thousand Cankers Disease. USDA Forest Service, Northeastern Area State and Private Forestry Pest Alert. NA-PR-02e10, originally published May 2010. http://www.na.fs.fed.us/pubs/detail.cfm
Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337
Smreczyński S (1972) Klucze do oznaczania owadów Polski; Część´XIX: Chrząszcze—Coleoptera, zeszyt 98d: Ryjkowce - Curculionidae; podrodzina Curculioninae. Polskie Towarzystwo Entomologiczne, Warszawa
Tisserat N, Cranshaw W, Leatherman D, Utley C, Alexander K (2009) Black walnut mortality in Colorado caused by the walnut twig beetle and thousand cankers disease. Plant Health Prog. https://doi.org/10.1094/PHP-2009-0811-01-RS
Utley C, Nguyen T, Roubtsova T, Coggeshall M, Ford TM, Grauke LJ, Graves AD, Lesile ChA, McKenna J, Woeste K, Yaghmour MA, Seybold SJ, Bostock RM, Tisserat N (2013) Susceptibility of walnut and hickory species to Geosmithia morbida. Plant Dis 97:601–607
Veselská T, Skelton J, Kostovčík M, Hulcr J, Baldrian P, Chudíčková M, Cajthaml T, Vojtová T, Garcia-Fraile P, Kolařík M (2019) Adaptive traits of bark and ambrosia beetle-associated fungi. Fungal Ecol 41:165–176
White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Snisky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322
Acknowledgements
The authors gratefully acknowledge the financial support from the National Science Centre in Poland (contract No. UMO-2014/15/NZ9/00560).
Funding
This study was funded by the National Science Centre, Poland (contract No. UMO-2014/15/B/NZ9/00560) and by the Ministry of Science and Higher Education of the Republic of Poland. MK was supported by the grant BIOCEV CZ.1.05/1.1.00/02.0109.
Author information
Authors and Affiliations
Contributions
BS designed the study, collecting samples, identification of fungi, performed the pathogenic test and the phenotypic characterization, wrote the original draft; RJ designed the study, performed the phenotypic and molecular characterization, edited the original draft; MK performed the phenotypic and molecular characterization; the analysis of molecular and taxonomic data, deposited fungal cultures, edited the original draft.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Strzałka, B., Kolařík, M. & Jankowiak, R. Geosmithia associated with hardwood-infesting bark and ambrosia beetles, with the description of three new species from Poland. Antonie van Leeuwenhoek 114, 169–194 (2021). https://doi.org/10.1007/s10482-020-01510-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-020-01510-6